Exploration for reliable radiographic assessment method for hinge-like hypermobility at atlanto-occipital joint

Exploration for reliable radiographic assessment method for hinge-like hypermobility at... Eur Spine J (2018) 27:1303–1308 https://doi.org/10.1007/s00586-017-5349-3 ORIGINAL ARTICLE Exploration for reliable radiographic assessment method for hinge‑like hypermobility at atlanto‑occipital joint 1,4 2,4 2,4 3,4 Shinjiro Kaneko  · Ken Ishii  · Kota Watanabe  · Takashi Tsuji  · 2,4 2,4 1,4 1,4 Masaya Nakamura  · Morio Matsumoto  · Yoshiyuki Yato  · Takashi Asazuma   Received: 11 December 2016 / Revised: 13 May 2017 / Accepted: 13 October 2017 / Published online: 20 October 2017 © The Author(s) 2017. This article is an open access publication Abstract angles using dynamic-MRI. Evaluation of O-C1 instability Purpose Hinge-like hyper-mobility is occasionally is important especially when we perform surgical treatment observed at the atlanto-occipital (O-C1) joint. However, it for diseases with upper cervical instability (such as retro- has not been clear if this kind of hinge-like hyper-mobility odontoid pseudotumor). We consider that the current study at the O-C1 joint should be regarded as “pathologic”, or provides important information in such a case. referred to as “instability”. To solve this issue, we aimed to establish a reliable radiographic assessment method for this Keywords Atlanto-occipital (O-C1) instability · specific type of O-C1 instability and figure out the “standard Classification · Radiographic assessment method · value” for the range of motion (ROM) of the O-C1 joint. Dynamic magnetic resonance imaging · O-C1 angle Methods To figure out the standard range of the O-C1 angle, we acquired magnetic resonance imaging (MRI) sag- ittal views of the cervical spine for 157 healthy volunteers Introduction [average: 37.4 year-old (yo)] without spine diseases, at neu- tral, maximum flexion and maximum extension positions. Atlanto-occipital (O-C1) instability [2, 3, 5, 7, 8, 11–14, 16, Results The average value (AVE) for ROM of O-C1 angle 19–23, 25, 26] is generally caused by trauma [2, 5, 7, 11–13, was 9.91°. The standard value for ROM of O-C1 angle was 19, 21, 25]. Non-traumatic O-C1 instability [3, 8, 14, 16, 20, calculated as 0°–21°. There was no statistically significant 22, 23, 26], which is less common, is usually associated with gender difference. We also found that the older popula - rheumatoid arthritis (RA) [16, 20] or ankylosing spondylitis tion (≧  40  yo) significantly had a larger ROM of O-C1 (AS) [8, 22]. It can also be associated with Down syndrome angle (AVE: 11.72°) compared to the younger population [3, 11, 23] or infectious diseases [26]. (< 40 yo) (AVE: 8.99°). It has been known that there are several types of O-C1 Conclusions We consider that hinge-like instability at instability. We consider that O-C1 instability can be classi- O-C1 joint, which cannot be assessed by measuring Pow- fied into three types (Table  1). The first type is the anterior ers ratio, can be assessed by measuring the range of O-C1 hyper-shift of the occiput (Type 1). This type has been the most-reported type and is usually accompanied with trauma [2, 5, 7, 11, 12, 19, 21, 25]. The second type is character- * Shinjiro Kaneko ized by posterior hyper-shift of the occiput (Type 2), which ShinjiroKaneko@gmail.com is often accompanied with RA [16, 20]. These two types Department of Orthopaedic Surgery, National Hospital of O-C1 instability have been termed as atlanto-occipital Organization Murayama Medical Center, Tokyo, Japan subluxation (AOS) [2, 5, 7, 8, 12, 14, 16, 20–23, 25, 26] and Department of Orthopaedic Surgery, Keio University School commonly been diagnosed by measuring Powers ratio [19]. of Medicine, Tokyo, Japan Other than these two types, we sometimes observe Department of Orthopaedic Surgery, Fujita Health University hinge-like hyper-mobility at the O-C1 joint (Type 3). This Hospital, Toyoake, Japan type of O-C1 instability is occasionally accompanied with Keio Spine Research Group (KSRG), Tokyo, Japan retro-odontoid pseudotumor (ROP) [1, 4, 6, 15, 17, 18, 24, Vol.:(0123456789) 1 3 1304 Eur Spine J (2018) 27:1303–1308 Table 1 Our classification of O-C1 instability and each type’s characteristics Type 1 Type 2 Type 3 Type of O-C1 instability Anterior hyper-shift of the occiput Posterior hyper-shift of the Hinge-like hyper-mobility at O-C1 occiput joint Representative case report in the Georgopoulos et al. [11] Romanowski et al. [20] literatures Adequate method for diagnosis Powers ratio (> approx. 1) Powers ratio (< approx. 0.5) Our study (measuring ROM of O-C1 angle) Adequate tool(s) for diagnosis Dynamic-MRI (or CT) or (>) Xp Dynamic-MRI (or CT) or (>) Xp Dynamic-MRI (or CT) Representative etiology Mostly trauma One of the consequences of RA Often accompanied with retro- odontoid pseudo-tumor 27]. However, it has not been clear if this kind of hinge- atlas (Fig. 1a). The centers of the anterior and posterior like hyper-mobility at the O-C1 joint should be regarded arches were defined as the cross-point of the longest and as “pathologic”, or referred to as “instability”. If we can shortest axis of the sagittal view of anterior and posterior establish a reliable radiographic assessment method for arches. The structures of the bones are usually outlined O-C1 instability and figure out the “standard value” for the by low intensity area in MRI T2-weighted images. This range of motion (ROM) of the O-C1 joint, we may be able low intensity area sometimes cannot be distinguished from to solve this issue. other attaching structures such as ligaments, so that the measurements were performed by selecting relatively high intensity area as the outlines of the bones. Materials and methods To figure out the standard range of the O-C1 angle, we acquired T2-weighted dynamic-MRI of the cervical spine Using sagittal view T2 weighted-magnetic resonance for 157 healthy volunteers (22–65 years old (yso), aver- imaging (MRI), we defined O-C1 angle as the angle age: 37.4 yso) without spine diseases, at neutral, maximum formed by (1) the line between the anterior and posterior flexion and maximum extension positions (Fig.  1b–d). To borders of the foramen magnum, and (2) a line through make sure that the flexion and extension is at the person’s the centers of the anterior and posterior arches of the Fig. 1 Method for measuring O-C1 angle. a We defined O-C1 angle as the angle formed by (1) the line between the anterior and posterior borders of the foramen magnum, and (2) a line through the centers of the anterior and posterior arches of the atlas and measured it using T2-weighted sagittal view MRI. b–d We acquired T2-weighted dynamic-MRI of the cervi- cal spine at maximum flexion (b), neutral (c), and maximum extension positions (d) 1 3 Eur Spine J (2018) 27:1303–1308 1305 maximum, an assisting device was used to hold the per- All the process of the current study was reviewed and son’s head position. approved by the Institutional Review Board at our institute. Intra-observer reliability was assessed by performing the measurement once a day for 3 consecutive days, obtaining a total of three measurements. For intra-observer reliability Results assessment, 15 different samples were used. Inter-observer reliability was assessed with six surgeons including three We first evaluated the intra-observer and inter-observer board-certificated instructors in spinal surgery (instructors) reliability of our measurement method of the O-C1 angle. and three under-training-spinal surgeons (fellows). For inter- The data of intra-observer reliability is shown in Table 2A. observer reliability assessment, 15 different samples and While ICC(1,3) was 0.996, ICC(1,1) was 0.989 indicating 45 images in total were used for each measurer to measure that data acquired by single measurement has an excellent O-C1 angle at 3 different positions in each sample. Inter- enough reliability. Considering this data, we used data from observer and intra-observer reliability were estimated by single measurements in the following inter-observer reli- calculating intra-class correlation coefficients (ICC) at 95% ability analysis. confidence intervals using IBM SPSS statistics (version 24) As mentioned, inter-observer reliability was assessed by software. six surgeons including three board-certificated instructors in We calculated O-C1 ROM by subtracting the O-C1 angle spinal surgery (instructors) and three under-training-spinal at maximum extension from that of maximum flexion. Stu- surgeons (fellows). Assessment was performed in all three dent t test was used for statistical analysis in the comparative different positions: neutral, maximum flexion and maximum analyses. extension positions. Table 2 Intra-observer reliability and inter-observer reliability analyses of O-C1 angle measurement A. Intra-observer reliability Intra-observer reliability 95% confidence interval p value ICC(1,1) 0.989 0.973–0.996 < 0.01 ICC(1,3) 0.996 0.991–0.999 < 0.01 B: Inter-observer reliability analysis of board-certificated instructors in spinal surgery (instructors) Inter-observer reliability (instructors) 95% confidence interval p-value Neutral position  ICC(2,1) 0.933 0.850–0.975 < 0.01  ICC(2,3) 0.976 0.944–0.991 < 0.01 Maximum flexion position  ICC(2,1) 0.973 0.938–0.990 < 0.01  ICC(2,3) 0.991 0.978–0.997 < 0.01 Maximum extension position  ICC(2,1) 0.959 0.907–0.985 < 0.01  ICC(2,3) 0.986 0.967–0.995 < 0.01 C: Inter-observer reliability analysis of under-training-spinal surgeons (fellows) Inter-observer reliability (fellows) 95% confidence interval p-value Neutral position  ICC(2,1) 0.972 0.936–0.990 < 0.01  ICC(2,3) 0.990 0.978–0.997 < 0.01 Maximum flexion position  ICC(2,1) 0.915 0.814–0.968 < 0.01  ICC(2,3) 0.970 0.929–0.989 < 0.01 Maximum extension position  ICC(2,1) 0.944 0.870–0.979 < 0.01  ICC(2,3) 0.981 0.953–0.993 < 0.01 1 3 1306 Eur Spine J (2018) 27:1303–1308 Table 3 O-C1 angle of the whole population of the study The average value (AVE) of the whole population of the study for O-C1 angle at neutral, maximum flexion and O-C1 angle At neutral At At maximum ROM maximum extension positions was 5.06°, 9.27° and − 0.64°, (°) position maximum extension flexion position respectively (Table 3). AVE for ROM of the O-C1 angle was position calculated as 9.91° (Table 3). When we regard the standard value for ROM of O-C1 angle as the value within the range Overall 5.06 ± 0.48 9.27 ± 0.49 − 0.64 ± 0.48 9.91 ± 0.45 (n = 157) of ± 2SD, it was calculated as 0°–21°. We also examined whether there is a significant differ - AVE ± SEM is presented in the table. When we regard the standard ence between males and females. Average age of males and value for ROM of O-C1 angle as the value within the range of ± 2SD, females was 36.32 and 39.58 yo, respectively. There was no it was calculated as 0°–21° statistically significant difference. AVE for ROM of O-C1 angle was 10.07° in males and 9.60° in females (Table 4). The data of inter-observer reliability acquired from There was no statistically significant difference between the instructors are shown in Table  2B. At neutral position, two groups. ICC(2,1) was 0.933 and ICC(2,3) was 0.976. At maxi- Next, we examined whether there is a significant differ - mum flexion position, ICC(2,1) was 0.973 and ICC(2,3) ence between the older population (≧ 40 yo) and the younger was 0.991. At maximum extension position, ICC(2,1) was population (< 40 yo). We found that the older population 0.959 and ICC(2,3) was 0.986. These values indicate that significantly had a larger ROM of O-C1 angle (AVE: these measurements have excellent inter-observer reliabil- 11.72°) compared to the younger population (AVE: 8.99°) ity at all three positions. The data of inter-observer reli- (p = 0.0038) (Table 5). ability acquired from fellows are shown in Table 2C. These values also indicate that the measurements have excellent inter-observer reliability at all three positions. Discussion Taken together, we considered that this measurement method of O-C1 angle is reliable enough to explore the The standard ROM of the O-C1 joint has not been clear “standard value” for the range of motion (ROM) of the partly because the precision of measurements obtained O-C1 joint with good reproducibility and feasibility. from dynamic-X-ray films, especially those using occipi- To figure out the standard range of the O-C1 angle, we tal landmarks is limited by the relatively poor resolution. measured O-C1 angle for 157 healthy volunteers at neu- We consider that Type 3 O-C1 instability, which cannot be tral, maximum flexion and maximum extension positions. assessed by measuring Powers ratio [19], can be assessed by measuring the range of O-C1 angles using dynamic-MRI. In Table 4 O-C1 angle of males O-C1 angle (°) At neutral position At maximum flex- At maximum exten- ROM and females ion position sion position Males (n = 105) 5.89 ± 0.59 9.96 ± 0.57 − 0.10 ± 0.60 10.07 ± 0.56 Females (n = 52) 3.23 ± 0.75 7.88 ± 0.88 − 1.71 ± 0.77 9.60 ± 0.77 AVE  ±  SEM is presented in the table. No statistically significant difference was found between the two groups Table 5 O-C1 angle of the O-C1 angle (°) At neutral position At maximum At maximum ROM older population (≧ 40 yso) and flexion position extension position the younger population (< 40 yso) 4.70 ± 0.55 8.58 ± 0.56 − 0.41 ± 0.58 8.99 ± 0.49 Younger population (< 40 yso) (n = 104) (73 males and 31 females) Older population (≧ 40 5.60 ± 0.92 10.64 ± 0.91 − 1.08 ± 0.83 11.72 ± 0.90* yso) (n = 53) (32 males and 21 females) AVE ± SEM is presented in the table. The older population significantly had a larger ROM of O-C1 angle compared to the younger population (*p = 0.0038) 1 3 Eur Spine J (2018) 27:1303–1308 1307 addition, assessment using dynamic-MRI has an advantage and Tanaka et al. suggested that AAS does not accompany that it can be performed without exposure to radiation. ROP in some cases [6, 24]. Yet, the underlying mechanism Dvorak et al. examined age and gender related stand- for ROP formation without AAS has not been well-eluci- ard motion of the cervical spine. By developing a clinical dated. ROP is also reported to be associated with diffuse method for measuring three-dimensional motion of the cer- idiopathic skeletal hyperostosis (DISH) [4, 15] at times. vical spine using a specific device, they obtained the stand- Taken together, O-C1 instability has been thought to be ard values for passive examinations of flexion–extension, one of the possible causes of ROP without AAS. However, lateral bending, rotation, rotation out of maximum flexion, there has been no clear evidence of it due to the lack of reli- and rotation out of maximum extension and analyzed them able radiographic assessment methods for O-C1 instability. for each gender in a group of 150 normal subjects. Results When performing arthrodesis for ROP, evaluation of O-C1 of rotation out of maximum flexion suggest and supported instability is important to decide if the fusion range should their earlier conclusions that the rotation of the C1–C2 include O-C1 [1, 4, 17, 27]. Commonly, the type of O-C1 segment does not decrease with age, but rather increases instability accompanied with ROP is the hinge-like hyper- slightly. They concluded that it may be the compensation mobility at the O-C1 joint. It has not been clear whether this for the overall decreased motion in the lower segments [10]. kind of hinge-like hyper-mobility at the O-C1 joint should In this study, we found that the older population (≧ 40 yo) be regarded as “pathologic”, or referred to as “instability”. significantly had a larger ROM of O-C1 angle compared to In this study, we proposed a reliable radiographic assess- the younger population (< 40 yo). We consider that this also ment method for Type 3 O-C1 instability and g fi ured out the may be the compensation for the overall decreased motion “standard value” for the range of motion (ROM) of the O-C1 in the lower segments. joint. We consider that the current study provides important In the craniocervical joint, the alar and transverse liga- information for such a case. ments provide much of the stability in the healthy spine. As mentioned, ROP sometimes is associated with DISH These ligaments can be damaged by a high-energy decelera- [4, 15]. O-C1 instability, as the compensation for the overall tion force that causes hyperextension–flexion. Chaput et al. decreased motion in the lower segments, may be the under- performed radiographic analysis to detect these traumatic lying mechanism of ROP formation in cases associated ligamentous injuries [5]. The degenerative change on the with DISH. Future study using the radiographic method we O-C1 joint may also affect the O-C1 ligaments and its joint proposed in the current study may elucidate the underlying stability. The alar ligament restrains rotation of the upper mechanism of ROP formation with DISH, or those without cervical spine, whereas the transverse ligament restricts flex- AAS. ion as well as anterior displacement of the atlas [9]. A lesion O-C1 instability can be also associated with rheumatoid in one or both structures can produce damage to the neural arthritis (RA) [16, 20] ankylosing spondylitis (AS) [8, 22], structures and/or cause pain. Dvorak et al. investigated the Down syndrome [3, 11, 23] or infectious diseases [26], as possible role of each of these ligaments by a mechanical mentioned. Future study using the radiographic method we and histologic study of the upper cervical spine. Using the proposed in the current study may also contribute to clarify bone–ligament–bone complex of the alar and transverse liga- the underlying mechanism of these diseases. ments, they performed a uniaxial mechanical testing in the Acknowledgements We gratefully acknowledge Dr. Yuji Nishiwaki, specimens. The result reported that the transverse ligaments Dr. Hitoshi Kono, Dr. Akio Iwanami, Dr. Junichi Yamane, Dr. Takashi had greater strength in vitro strength compared with the alar Kato, Dr. Taro Umezu, Dr. Yasuhiro Kamata and Dr. Takahiro Ishizaka, ligaments. They also revealed a mainly collagenous nature who assisted this study. We also gratefully acknowledge those who accepted to be healthy volunteers in this study, those who performed in these ligaments through histologic analysis and men- MRI scanning and all other people who involved in this study. tioned that clinical evidence (broken odontoid processes) suggests that the transverse ligament is strong enough to Compliance with ethical standards withstand physiologic loads. They also mentioned that the alar ligament, on the other hand, due to its lower strength Conflict of interest No conflict of interest to declare. and its axial direction of loading, might be prone to injury and therefore require stabilization of the appropriate verte- Open Access This article is distributed under the terms of the bra more often than normally assumed [9]. Future detailed Creative Commons Attribution 4.0 International License (http://crea- tivecommons.org/licenses/by/4.0/), which permits unrestricted use, analysis is necessary to elucidate the degenerative changes distribution, and reproduction in any medium, provided you give appro- in O-C1 joint in stability occurring in the older population. priate credit to the original author(s) and the source, provide a link to ROP is commonly associated with upper cervical instabil- the Creative Commons license, and indicate if changes were made. ity and surgical treatment for ROP includes arthrodesis. His- torically, ROP had been well-known to be accompanied with atlantoaxial subluxation (AAS). However, Chikuda et al. 1 3 1308 Eur Spine J (2018) 27:1303–1308 14. Hettiaratchy S, Ning C, Sabin I (1998) Nontraumatic atlanto- References occipital and atlantoaxial rotatory subluxation: case report. Neu- rosurgery 43:164–165 1. Barbagallo GM, Certo F, Visocchi M et al (2013) Disappearance 15. 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Exploration for reliable radiographic assessment method for hinge-like hypermobility at atlanto-occipital joint

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Abstract

Eur Spine J (2018) 27:1303–1308 https://doi.org/10.1007/s00586-017-5349-3 ORIGINAL ARTICLE Exploration for reliable radiographic assessment method for hinge‑like hypermobility at atlanto‑occipital joint 1,4 2,4 2,4 3,4 Shinjiro Kaneko  · Ken Ishii  · Kota Watanabe  · Takashi Tsuji  · 2,4 2,4 1,4 1,4 Masaya Nakamura  · Morio Matsumoto  · Yoshiyuki Yato  · Takashi Asazuma   Received: 11 December 2016 / Revised: 13 May 2017 / Accepted: 13 October 2017 / Published online: 20 October 2017 © The Author(s) 2017. This article is an open access publication Abstract angles using dynamic-MRI. Evaluation of O-C1 instability Purpose Hinge-like hyper-mobility is occasionally is important especially when we perform surgical treatment observed at the atlanto-occipital (O-C1) joint. However, it for diseases with upper cervical instability (such as retro- has not been clear if this kind of hinge-like hyper-mobility odontoid pseudotumor). We consider that the current study at the O-C1 joint should be regarded as “pathologic”, or provides important information in such a case. referred to as “instability”. To solve this issue, we aimed to establish a reliable radiographic assessment method for this Keywords Atlanto-occipital (O-C1) instability · specific type of O-C1 instability and figure out the “standard Classification · Radiographic assessment method · value” for the range of motion (ROM) of the O-C1 joint. Dynamic magnetic resonance imaging · O-C1 angle Methods To figure out the standard range of the O-C1 angle, we acquired magnetic resonance imaging (MRI) sag- ittal views of the cervical spine for 157 healthy volunteers Introduction [average: 37.4 year-old (yo)] without spine diseases, at neu- tral, maximum flexion and maximum extension positions. Atlanto-occipital (O-C1) instability [2, 3, 5, 7, 8, 11–14, 16, Results The average value (AVE) for ROM of O-C1 angle 19–23, 25, 26] is generally caused by trauma [2, 5, 7, 11–13, was 9.91°. The standard value for ROM of O-C1 angle was 19, 21, 25]. Non-traumatic O-C1 instability [3, 8, 14, 16, 20, calculated as 0°–21°. There was no statistically significant 22, 23, 26], which is less common, is usually associated with gender difference. We also found that the older popula - rheumatoid arthritis (RA) [16, 20] or ankylosing spondylitis tion (≧  40  yo) significantly had a larger ROM of O-C1 (AS) [8, 22]. It can also be associated with Down syndrome angle (AVE: 11.72°) compared to the younger population [3, 11, 23] or infectious diseases [26]. (< 40 yo) (AVE: 8.99°). It has been known that there are several types of O-C1 Conclusions We consider that hinge-like instability at instability. We consider that O-C1 instability can be classi- O-C1 joint, which cannot be assessed by measuring Pow- fied into three types (Table  1). The first type is the anterior ers ratio, can be assessed by measuring the range of O-C1 hyper-shift of the occiput (Type 1). This type has been the most-reported type and is usually accompanied with trauma [2, 5, 7, 11, 12, 19, 21, 25]. The second type is character- * Shinjiro Kaneko ized by posterior hyper-shift of the occiput (Type 2), which ShinjiroKaneko@gmail.com is often accompanied with RA [16, 20]. These two types Department of Orthopaedic Surgery, National Hospital of O-C1 instability have been termed as atlanto-occipital Organization Murayama Medical Center, Tokyo, Japan subluxation (AOS) [2, 5, 7, 8, 12, 14, 16, 20–23, 25, 26] and Department of Orthopaedic Surgery, Keio University School commonly been diagnosed by measuring Powers ratio [19]. of Medicine, Tokyo, Japan Other than these two types, we sometimes observe Department of Orthopaedic Surgery, Fujita Health University hinge-like hyper-mobility at the O-C1 joint (Type 3). This Hospital, Toyoake, Japan type of O-C1 instability is occasionally accompanied with Keio Spine Research Group (KSRG), Tokyo, Japan retro-odontoid pseudotumor (ROP) [1, 4, 6, 15, 17, 18, 24, Vol.:(0123456789) 1 3 1304 Eur Spine J (2018) 27:1303–1308 Table 1 Our classification of O-C1 instability and each type’s characteristics Type 1 Type 2 Type 3 Type of O-C1 instability Anterior hyper-shift of the occiput Posterior hyper-shift of the Hinge-like hyper-mobility at O-C1 occiput joint Representative case report in the Georgopoulos et al. [11] Romanowski et al. [20] literatures Adequate method for diagnosis Powers ratio (> approx. 1) Powers ratio (< approx. 0.5) Our study (measuring ROM of O-C1 angle) Adequate tool(s) for diagnosis Dynamic-MRI (or CT) or (>) Xp Dynamic-MRI (or CT) or (>) Xp Dynamic-MRI (or CT) Representative etiology Mostly trauma One of the consequences of RA Often accompanied with retro- odontoid pseudo-tumor 27]. However, it has not been clear if this kind of hinge- atlas (Fig. 1a). The centers of the anterior and posterior like hyper-mobility at the O-C1 joint should be regarded arches were defined as the cross-point of the longest and as “pathologic”, or referred to as “instability”. If we can shortest axis of the sagittal view of anterior and posterior establish a reliable radiographic assessment method for arches. The structures of the bones are usually outlined O-C1 instability and figure out the “standard value” for the by low intensity area in MRI T2-weighted images. This range of motion (ROM) of the O-C1 joint, we may be able low intensity area sometimes cannot be distinguished from to solve this issue. other attaching structures such as ligaments, so that the measurements were performed by selecting relatively high intensity area as the outlines of the bones. Materials and methods To figure out the standard range of the O-C1 angle, we acquired T2-weighted dynamic-MRI of the cervical spine Using sagittal view T2 weighted-magnetic resonance for 157 healthy volunteers (22–65 years old (yso), aver- imaging (MRI), we defined O-C1 angle as the angle age: 37.4 yso) without spine diseases, at neutral, maximum formed by (1) the line between the anterior and posterior flexion and maximum extension positions (Fig.  1b–d). To borders of the foramen magnum, and (2) a line through make sure that the flexion and extension is at the person’s the centers of the anterior and posterior arches of the Fig. 1 Method for measuring O-C1 angle. a We defined O-C1 angle as the angle formed by (1) the line between the anterior and posterior borders of the foramen magnum, and (2) a line through the centers of the anterior and posterior arches of the atlas and measured it using T2-weighted sagittal view MRI. b–d We acquired T2-weighted dynamic-MRI of the cervi- cal spine at maximum flexion (b), neutral (c), and maximum extension positions (d) 1 3 Eur Spine J (2018) 27:1303–1308 1305 maximum, an assisting device was used to hold the per- All the process of the current study was reviewed and son’s head position. approved by the Institutional Review Board at our institute. Intra-observer reliability was assessed by performing the measurement once a day for 3 consecutive days, obtaining a total of three measurements. For intra-observer reliability Results assessment, 15 different samples were used. Inter-observer reliability was assessed with six surgeons including three We first evaluated the intra-observer and inter-observer board-certificated instructors in spinal surgery (instructors) reliability of our measurement method of the O-C1 angle. and three under-training-spinal surgeons (fellows). For inter- The data of intra-observer reliability is shown in Table 2A. observer reliability assessment, 15 different samples and While ICC(1,3) was 0.996, ICC(1,1) was 0.989 indicating 45 images in total were used for each measurer to measure that data acquired by single measurement has an excellent O-C1 angle at 3 different positions in each sample. Inter- enough reliability. Considering this data, we used data from observer and intra-observer reliability were estimated by single measurements in the following inter-observer reli- calculating intra-class correlation coefficients (ICC) at 95% ability analysis. confidence intervals using IBM SPSS statistics (version 24) As mentioned, inter-observer reliability was assessed by software. six surgeons including three board-certificated instructors in We calculated O-C1 ROM by subtracting the O-C1 angle spinal surgery (instructors) and three under-training-spinal at maximum extension from that of maximum flexion. Stu- surgeons (fellows). Assessment was performed in all three dent t test was used for statistical analysis in the comparative different positions: neutral, maximum flexion and maximum analyses. extension positions. Table 2 Intra-observer reliability and inter-observer reliability analyses of O-C1 angle measurement A. Intra-observer reliability Intra-observer reliability 95% confidence interval p value ICC(1,1) 0.989 0.973–0.996 < 0.01 ICC(1,3) 0.996 0.991–0.999 < 0.01 B: Inter-observer reliability analysis of board-certificated instructors in spinal surgery (instructors) Inter-observer reliability (instructors) 95% confidence interval p-value Neutral position  ICC(2,1) 0.933 0.850–0.975 < 0.01  ICC(2,3) 0.976 0.944–0.991 < 0.01 Maximum flexion position  ICC(2,1) 0.973 0.938–0.990 < 0.01  ICC(2,3) 0.991 0.978–0.997 < 0.01 Maximum extension position  ICC(2,1) 0.959 0.907–0.985 < 0.01  ICC(2,3) 0.986 0.967–0.995 < 0.01 C: Inter-observer reliability analysis of under-training-spinal surgeons (fellows) Inter-observer reliability (fellows) 95% confidence interval p-value Neutral position  ICC(2,1) 0.972 0.936–0.990 < 0.01  ICC(2,3) 0.990 0.978–0.997 < 0.01 Maximum flexion position  ICC(2,1) 0.915 0.814–0.968 < 0.01  ICC(2,3) 0.970 0.929–0.989 < 0.01 Maximum extension position  ICC(2,1) 0.944 0.870–0.979 < 0.01  ICC(2,3) 0.981 0.953–0.993 < 0.01 1 3 1306 Eur Spine J (2018) 27:1303–1308 Table 3 O-C1 angle of the whole population of the study The average value (AVE) of the whole population of the study for O-C1 angle at neutral, maximum flexion and O-C1 angle At neutral At At maximum ROM maximum extension positions was 5.06°, 9.27° and − 0.64°, (°) position maximum extension flexion position respectively (Table 3). AVE for ROM of the O-C1 angle was position calculated as 9.91° (Table 3). When we regard the standard value for ROM of O-C1 angle as the value within the range Overall 5.06 ± 0.48 9.27 ± 0.49 − 0.64 ± 0.48 9.91 ± 0.45 (n = 157) of ± 2SD, it was calculated as 0°–21°. We also examined whether there is a significant differ - AVE ± SEM is presented in the table. When we regard the standard ence between males and females. Average age of males and value for ROM of O-C1 angle as the value within the range of ± 2SD, females was 36.32 and 39.58 yo, respectively. There was no it was calculated as 0°–21° statistically significant difference. AVE for ROM of O-C1 angle was 10.07° in males and 9.60° in females (Table 4). The data of inter-observer reliability acquired from There was no statistically significant difference between the instructors are shown in Table  2B. At neutral position, two groups. ICC(2,1) was 0.933 and ICC(2,3) was 0.976. At maxi- Next, we examined whether there is a significant differ - mum flexion position, ICC(2,1) was 0.973 and ICC(2,3) ence between the older population (≧ 40 yo) and the younger was 0.991. At maximum extension position, ICC(2,1) was population (< 40 yo). We found that the older population 0.959 and ICC(2,3) was 0.986. These values indicate that significantly had a larger ROM of O-C1 angle (AVE: these measurements have excellent inter-observer reliabil- 11.72°) compared to the younger population (AVE: 8.99°) ity at all three positions. The data of inter-observer reli- (p = 0.0038) (Table 5). ability acquired from fellows are shown in Table 2C. These values also indicate that the measurements have excellent inter-observer reliability at all three positions. Discussion Taken together, we considered that this measurement method of O-C1 angle is reliable enough to explore the The standard ROM of the O-C1 joint has not been clear “standard value” for the range of motion (ROM) of the partly because the precision of measurements obtained O-C1 joint with good reproducibility and feasibility. from dynamic-X-ray films, especially those using occipi- To figure out the standard range of the O-C1 angle, we tal landmarks is limited by the relatively poor resolution. measured O-C1 angle for 157 healthy volunteers at neu- We consider that Type 3 O-C1 instability, which cannot be tral, maximum flexion and maximum extension positions. assessed by measuring Powers ratio [19], can be assessed by measuring the range of O-C1 angles using dynamic-MRI. In Table 4 O-C1 angle of males O-C1 angle (°) At neutral position At maximum flex- At maximum exten- ROM and females ion position sion position Males (n = 105) 5.89 ± 0.59 9.96 ± 0.57 − 0.10 ± 0.60 10.07 ± 0.56 Females (n = 52) 3.23 ± 0.75 7.88 ± 0.88 − 1.71 ± 0.77 9.60 ± 0.77 AVE  ±  SEM is presented in the table. No statistically significant difference was found between the two groups Table 5 O-C1 angle of the O-C1 angle (°) At neutral position At maximum At maximum ROM older population (≧ 40 yso) and flexion position extension position the younger population (< 40 yso) 4.70 ± 0.55 8.58 ± 0.56 − 0.41 ± 0.58 8.99 ± 0.49 Younger population (< 40 yso) (n = 104) (73 males and 31 females) Older population (≧ 40 5.60 ± 0.92 10.64 ± 0.91 − 1.08 ± 0.83 11.72 ± 0.90* yso) (n = 53) (32 males and 21 females) AVE ± SEM is presented in the table. The older population significantly had a larger ROM of O-C1 angle compared to the younger population (*p = 0.0038) 1 3 Eur Spine J (2018) 27:1303–1308 1307 addition, assessment using dynamic-MRI has an advantage and Tanaka et al. suggested that AAS does not accompany that it can be performed without exposure to radiation. ROP in some cases [6, 24]. Yet, the underlying mechanism Dvorak et al. examined age and gender related stand- for ROP formation without AAS has not been well-eluci- ard motion of the cervical spine. By developing a clinical dated. ROP is also reported to be associated with diffuse method for measuring three-dimensional motion of the cer- idiopathic skeletal hyperostosis (DISH) [4, 15] at times. vical spine using a specific device, they obtained the stand- Taken together, O-C1 instability has been thought to be ard values for passive examinations of flexion–extension, one of the possible causes of ROP without AAS. However, lateral bending, rotation, rotation out of maximum flexion, there has been no clear evidence of it due to the lack of reli- and rotation out of maximum extension and analyzed them able radiographic assessment methods for O-C1 instability. for each gender in a group of 150 normal subjects. Results When performing arthrodesis for ROP, evaluation of O-C1 of rotation out of maximum flexion suggest and supported instability is important to decide if the fusion range should their earlier conclusions that the rotation of the C1–C2 include O-C1 [1, 4, 17, 27]. Commonly, the type of O-C1 segment does not decrease with age, but rather increases instability accompanied with ROP is the hinge-like hyper- slightly. They concluded that it may be the compensation mobility at the O-C1 joint. It has not been clear whether this for the overall decreased motion in the lower segments [10]. kind of hinge-like hyper-mobility at the O-C1 joint should In this study, we found that the older population (≧ 40 yo) be regarded as “pathologic”, or referred to as “instability”. significantly had a larger ROM of O-C1 angle compared to In this study, we proposed a reliable radiographic assess- the younger population (< 40 yo). We consider that this also ment method for Type 3 O-C1 instability and g fi ured out the may be the compensation for the overall decreased motion “standard value” for the range of motion (ROM) of the O-C1 in the lower segments. joint. We consider that the current study provides important In the craniocervical joint, the alar and transverse liga- information for such a case. ments provide much of the stability in the healthy spine. As mentioned, ROP sometimes is associated with DISH These ligaments can be damaged by a high-energy decelera- [4, 15]. O-C1 instability, as the compensation for the overall tion force that causes hyperextension–flexion. Chaput et al. decreased motion in the lower segments, may be the under- performed radiographic analysis to detect these traumatic lying mechanism of ROP formation in cases associated ligamentous injuries [5]. The degenerative change on the with DISH. Future study using the radiographic method we O-C1 joint may also affect the O-C1 ligaments and its joint proposed in the current study may elucidate the underlying stability. The alar ligament restrains rotation of the upper mechanism of ROP formation with DISH, or those without cervical spine, whereas the transverse ligament restricts flex- AAS. ion as well as anterior displacement of the atlas [9]. A lesion O-C1 instability can be also associated with rheumatoid in one or both structures can produce damage to the neural arthritis (RA) [16, 20] ankylosing spondylitis (AS) [8, 22], structures and/or cause pain. Dvorak et al. investigated the Down syndrome [3, 11, 23] or infectious diseases [26], as possible role of each of these ligaments by a mechanical mentioned. Future study using the radiographic method we and histologic study of the upper cervical spine. Using the proposed in the current study may also contribute to clarify bone–ligament–bone complex of the alar and transverse liga- the underlying mechanism of these diseases. ments, they performed a uniaxial mechanical testing in the Acknowledgements We gratefully acknowledge Dr. Yuji Nishiwaki, specimens. The result reported that the transverse ligaments Dr. Hitoshi Kono, Dr. Akio Iwanami, Dr. Junichi Yamane, Dr. Takashi had greater strength in vitro strength compared with the alar Kato, Dr. Taro Umezu, Dr. Yasuhiro Kamata and Dr. Takahiro Ishizaka, ligaments. They also revealed a mainly collagenous nature who assisted this study. We also gratefully acknowledge those who accepted to be healthy volunteers in this study, those who performed in these ligaments through histologic analysis and men- MRI scanning and all other people who involved in this study. tioned that clinical evidence (broken odontoid processes) suggests that the transverse ligament is strong enough to Compliance with ethical standards withstand physiologic loads. They also mentioned that the alar ligament, on the other hand, due to its lower strength Conflict of interest No conflict of interest to declare. and its axial direction of loading, might be prone to injury and therefore require stabilization of the appropriate verte- Open Access This article is distributed under the terms of the bra more often than normally assumed [9]. Future detailed Creative Commons Attribution 4.0 International License (http://crea- tivecommons.org/licenses/by/4.0/), which permits unrestricted use, analysis is necessary to elucidate the degenerative changes distribution, and reproduction in any medium, provided you give appro- in O-C1 joint in stability occurring in the older population. priate credit to the original author(s) and the source, provide a link to ROP is commonly associated with upper cervical instabil- the Creative Commons license, and indicate if changes were made. ity and surgical treatment for ROP includes arthrodesis. His- torically, ROP had been well-known to be accompanied with atlantoaxial subluxation (AAS). However, Chikuda et al. 1 3 1308 Eur Spine J (2018) 27:1303–1308 14. Hettiaratchy S, Ning C, Sabin I (1998) Nontraumatic atlanto- References occipital and atlantoaxial rotatory subluxation: case report. Neu- rosurgery 43:164–165 1. Barbagallo GM, Certo F, Visocchi M et al (2013) Disappearance 15. 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J Clin Neurosci 16:99–103 genol 178:1261–1268 1 3

Journal

European Spine JournalSpringer Journals

Published: Oct 20, 2017

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